Global Diversity of Crabs (Crustacea: Decapoda: Brachyura) in Freshwater

Hydrobiologia (2008) 595:275–286 DOI 10.1007/s10750-007-9023-3

FRESHWATER ANIMAL DIVERSITY ASSESSMENT

Global diversity of crabs (Crustacea: Decapoda: Brachyura) in freshwater

Darren C. J. Yeo Æ Peter K. L. Ng Æ Neil Cumberlidge Æ Ce´lio Magalha˜es Æ Savel R. Daniels Æ Martha R. Campos

Springer Science+Business Media B.V. 2007

Abstract An assessment of the global freshwater true freshwater crab diversity including likely num- crab diversity is presented. A total of 1,476 species in bers of undescribed taxa suggest that the field remains 14 families are currently known from all zoogeo- largely in a ‘‘discovery’’ phase. Main ideas on the graphical regions (except Antarctica), including origins, diversification, and phylogeny of true fresh- 1,306 species in eight exclusively freshwater families water crabs are briefly discussed. The economic (Pseudothelphusidae, Trichodactylidae, Potamonauti- importance of freshwater crabs is also highlighted. dae, Deckeniidae, Platythelphusidae, Potamidae, Gecarcinucidae and Parathelphusidae). Estimates of Keywords Global assessment Á Freshwater crab Á Diversity Á Crustacea Á Decapoda Á Brachyura Á Species estimates Guest editors: E. V. Balian, C. Le´veˆque, H. Segers & K. Martens Freshwater Animal Diversity Assessment Introduction D. C. J. Yeo (&) Á P. K. L. Ng Department of Biological Sciences, National University Of the more than 6,700 known species of brachyuran of Singapore, 14 Science Drive 4, Singapore 117543, crabs, over 1,300 are true freshwater crabs. True Republic of Singapore freshwater crabs are regarded as those that have e-mail: [email protected] adopted freshwater, semi-terrestrial or terrestrial N. Cumberlidge modes of life, and are characterized by their ability Department of Biology, Northern Michigan University, to complete their life cycle independently of the Marquette, MI 49855, USA marine environment. These crabs are currently C. Magalha˜es assigned to eight exclusively freshwater families— Instituto Nacional de Pesquisas da Amazoˆnia, Caixa Pseudothelphusidae and Trichodactylidae (Mexico, postal 478, Manaus 69011-970 Amazonas, Brazil Central and South America), Potamonautidae (Africa and Madagascar), Deckeniidae and Platythelphusidae S. R. Daniels Department of Botany and Zoology, University of (East Africa), Potamidae (North Africa, southern Stellenbosch, Private Bag X1, Matieland 7602, Europe, Asia), Gecarcinucidae (Seychelles, Asia), South Africa and Parathelphusidae (Asia, Australasia) (Martin & Davis, 2001). Wholly or primary freshwater taxa M. R. Campos Instituto de Ciencias Naturales, Universidad Nacional de undergo direct development in which the large, yolky Colombia, Apartado Ae´reo, Bogota 103698, Colombia eggs hatch directly into juvenile crabs. Crabs found in 123 276 Hydrobiologia (2008) 595:275–286 freshwater also include numerous euryhaline species the forest floor litter or, in some cases, even climbing or secondary freshwater species from primarily trees (Ng, 1988; Ng & Tay, 2001; Cumberlidge et al., marine brachyuran families (e.g. Sesarmidae, Var- 2005). These freshwater crab species do not require unidae, Hymenosomatidae). Although these regular immersion in fresh water and can obtain freshwater species are fully adapted to freshwater/ water either from food, from drinking dew or casual terrestrial living, most do not have direct develop- water, or by capillary or osmotic uptake from moist ment in their life cycle (though highly abbreviated substrata. In the present chapter, such species are also development occurs in some) and most possess one or categorised as ‘‘freshwater-dependent’’ species (see more larval stages. The diversity of these taxa is also later; Table 1). assessed in this chapter (Tables 1 and 2), but the Freshwater crabs are primarily nocturnal, prefer- emphasis will be placed on the true freshwater crabs. ring to remain hidden during the day in sheltered Freshwater crabs belong to the Order Decapoda, the places and foraging mostly at night. They are mostly crustacean group that also includes lobsters, prawns, omnivorous scavengers, mainly feeding on plant crayfish and hermit crabs, which share the character- matter, but some are opportunistic carnivores, feeding istic presence of five pairs of thoracic legs (pereiopods). either on live prey such as fish and prawns or on dead In freshwater crabs the first pereiopods are modified as animals that they encounter (Ng, 1988; unpub.), and pincers (chelipeds), and the remaining four pairs are cannibalism is not uncommon (unpub.). Crabs them- relatively unspecialised walking legs (Fig. 1). The selves also constitute an important food resource for general body plan of freshwater crabs consists of a many species of fishes, birds, caymans, turtles and head, thorax and abdomen, with the head and thorax mammals (see Ng, 1988; Magalha˜es, 2003). (cephalothorax) covered by a broad carapace, and the abdomen reduced, flattened and flexed under the thoracic sternum. In adults, the male abdomen is slim Diversity and endemicity and narrow, and is either triangular or T-shaped, while the female abdomen is broad and round and covers Known global diversity nearly the entire thoracic sternum. Adult males bear two pairs of abdominal appendages (pleopods) that are There are currently a total of 238 genera and 1,476 modified into copulatory structures known as gono- species of known freshwater crabs from 14 families pods. Gonopod structure is taxonomically important, (including 1,306 true freshwater crab species in eight especially because the external morphology of fresh- families: Pseudothelphusidae, Trichodactylidae, water crabs tends to be rather conservative (see Ng, Potamonautidae, Deckeniidae, Platythelphusidae, Pota- 1988; Cumberlidge, 1999, for details). midae, Gecarcinucidae and Parathelphusidae) (as of 1st Freshwater crabs are found in the tropics and August 2006). The species and genus diversity of subtropics in most parts of the world, and occur in a primary as well as secondary freshwater species are wide variety of aquatic and terrestrial habitats. These listed by zoogeographical regions (sensu Cox, 2001)in decapods are present in almost all freshwater bodies, Tables 1 and 2, respectively. The total number of from clear, fast-flowing montane streams to sluggish species or genera of certain families listed in the last lowland rivers and streams, as well as in peat and column of Tables 1 and 2, respectively, do not tally freshwater swamps, stagnant ponds and rice fields, with the sum of species or genera from each zoogeo- and even in pools in tree holes and leaf axils. A fair graphical region because some taxa occur in more than number are also adapted to live in caves. Among the one region (see later, Tables 1 and 2 footnotes). primarily aquatic freshwater crabs, some (e.g. pota- Table 1 also lists separately the number of mids) are entirely adapted to living in fresh water, ‘‘freshwater-dependent’’ species (WDpt). In the and are not thought to be able to survive for long in context of the present volume, our assessment of salt water, while others (e.g. parathelphusids) are the freshwater crab species required grouping more tolerant of saline conditions, and can survive them into two broad ecological categories to reflect immersion in salt water for short periods of time. their different habitat preferences and degrees Terrestrial species may occur well away from of their association with freshwater habitats, viz., permanent freshwater sources, either moving among ‘‘real aquatic’’ species and ‘‘freshwater-dependent’’ 123 yrbooi 20)595:275–286 (2008) Hydrobiologia

Table 1 Global species diversity of freshwater crabs Family PA NA NT AT OL AU PAC Worldc Total FW WDpt Total FW WDpt Total FW WDpt Total FW WDpt Total FW WDpt Total FW WDpt Total FW WDpt Total FW WDpt

aPotamidaed 86 – – – – – 3 1 435 58 – – – – 509 59 aPotamonautidae – – – – – – 115 9 – – – – – – 115 9 aDeckeniidae – – – – – – 2 2 – – – – – – 2 2 aPlatythelphusidae – – – – – – 9 – – – – – – – 9 – aParathelphusidaee 4 – – – – – – – 243 14 52 8 – – 298 22 aGecarcinucidae – – – – – – 8 6 36 3 – – – – 44 9 aPseudothelphusidae – – 16 – 262 3 – – – – – – – – 278 3 aTrichodactylidae – – – – 51 – – – – – – – – – 51 – bGecarcinidaef ––3399998866882020 bHymenosomatidaeg 1–––1–1–8–9–3–22– bOcypodidae – – – – – – – – 2 – – – – – 2 – bSesarmidaeh 2 – – – 14 14 1 1 72 68 15 13 7 7 101 95 bGoneplacidae – – – – – – – – – – 2 – 2 – 4 – bVarunidaei 4–––3–1–14–5–4–21– Totalj 97 – 19 3 340 26 149 28 818 151 89 27 24 15 1476 219 Total FW: Aquatic + ’’freshwater dependent’’ species. WDpt: ‘‘freshwater-dependent’’ species (see text under ‘‘Known global diversity’’ for definition). PA: Palaearctic, NA: Nearctic, NT: Neotropical, AT: Afrotropical, OL: Oriental, AU: Australasian, PAC: Pacific Oceanic Islands a True (or primary) freshwater crab family b Secondary freshwater crab family c ‘‘World’’ refers to the actual total number of freshwater species, which may not necessarily be the sum of the totals for each zoogeographical region as some species occur in more than one region (see text) d Potamidae—15 species with Palaearctic/Oriental distributions e Parathelphusidae—1 species with Palaearctic/Oriental distribution f Gecarcinidae—13 species with various overlapping distributions (3 Nearctic/Neotropical + 4 Afrotropical/Neotropical + 4 Afrotropical/Oriental/Australasian/Pacific + 2 Oriental/Australasian/Pacific) g Hymenosomatidae—1 species with Neotropical/Australasian distribution h Sesarmidae—6 species with various overlapping distributions (1 Palaearctic/Oriental/Australasian + 1 Afrotropical/Oriental/Australasian + 1 Oriental/Australasian + 2 Oriental/Australasian/Pacific + 1 Australasian/Pacific) 123 i Varunidae—7 species with various overlapping distributions (3 Palaearctic/Oriental + 1 Palaearctic/Afrotropical/Oriental/Australasian/Pacific + 3 Oriental/Australasian) j Total—43 species with various overlapping distributions (see above for details) 277 278 Hydrobiologia (2008) 595:275–286

Table 2 Global genus diversity of freshwater crabs Family PA NA NT AT OL AU PAC Worldc aPotamidaed 9 – – 2 72 – – 78 aPotamonautidae – – – 12 – – – 12 aDeckeniidae – – – 1 – – – 1 aPlatythelphusidae – – – 1 – – – 1 aParathelphusidaee 1 – – – 35 9 – 42 aGecarcinucidae – – – 4 10 – – 14 aPseudothelphusidaef – 2 41 – – – – 41 aTrichodactylidae – – 15 – – – – 15 bGecarcinidaeg –2 3 4 4 4 4 6 bHymenosomatidaeh 1– 1 1 3 2 2 6 bOcypodidae – – – – 1 – – 1 bSesarmidaei 1– 3 1 7 4 3 10 bGoneplacidaej –– – – – 1 2 2 bVarunidaek 2– 2 1 7 4 2 9 Totall 14 4 65 27 139 24 13 238 PA: Palaearctic, NA: Nearctic, NT: Neotropical, AT: Afrotropical, OL: Oriental, AU: Australasian, PAC: Pacific Oceanic Islands a True (or primary) freshwater crab family b Secondary freshwater crab family c ‘‘World’’ refers to the actual total number of freshwater genera, which may not necessarily be the sum of the totals for each zoogeographical region as some genera occur in more than one region (see text) d Potamidae—5 genera with Palaearctic/Oriental distributions e Parathelphusidae—3 genera with various overlapping distributions (1 Palaearctic/Oriental + 2 Oriental/Australasian) f Pseudothelphusidae—2 genera with Nearctic/Neotropical distributions g Gecarcinidae—6 genera with various overlapping distributions (1 Nearctic/Neotropical + 1 Nearctic/Afrotropical/Neotropical/ Oriental/Australasian/Pacific + 1 Afrotropica/Neotropical + 2 Afrotropical/Oriental/Australasian/Pacific + 1 Oriental/Australasian/ Pacific) h Hymenosomatidae—2 genera with different overlapping distributions (1 Palaearctic/Oriental/Pacific + 1 Neotropical/Oriental/ Australasian) i Sesarmidae—4 genera with various overlapping distributions (1 Palaearctic/Oriental/Australasian + 1 Afrotropical/Oriental/ Australasian/Pacific + 2 Oriental/Australasian/Pacific) j Goneplacidae—1 genus with Australasian/Pacific distribution k Varunidae—6 genera with various overlapping distributions (1 Palaearctic/Oriental + 1 Palaearctic/Afrotropical/Oriental/ Australasian/Pacific + 3 Oriental/Australasian + 1 Oriental/Pacific) l Total—29 genera with various overlapping distributions (see above for details)

species. ‘‘Real aquatic’’ species are ones that are dependent on freshwater habitats to complete their life cycle i.e. part or all of the life cycle occurs in the water. Thus, adopting a practical approach, this study has included under ‘‘real aquatic’’ species all fully aquatic as well as semi-terrestrial species that are generally found in and around (or associated with) traditional freshwater environments (streams, rivers, lakes, ponds, swamps). Under ‘‘freshwater-dependent’’ species (WDpt), this work has included the Fig. 1 Habitus more terrestrial species in which the adults are not 123 Hydrobiologia (2008) 595:275–286 279

primarily found in and around (or associated with) a 160 s e traditional freshwater environments, but are never- i 140 c e

p 120 theless dependent on wet/humid terrestrial s

f Pseudothelphusidae o

100 environments for survival e.g. tree-climbing crabs, r e

b 80 forest ﬂoor dwellers, dry cave dwellers. These m u 60 n

include many so-called terrestrial crabs that have e

v 40 i t a juvenile stages that can occur in water. l 20 u

m 0 u

C 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 4 5 6 7 8 9 0 1 2 3 4 5 6 7 8 9 0 0 8 8 8 8 8 9 9 9 9 9 9 9 9 9 9 0 0 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 2 2 ------0 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 4 5 6 7 8 9 0 1 2 3 4 5 6 7 8 9 0 8 8 8 8 8 8 9 9 9 9 9 9 9 9 9 9 0 Estimated global biodiversity 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 2 Period

Two methods are proposed here for estimating the b 50

s 45 e global diversity of true freshwater crabs: i c

e 40

p Trichodactylidae

(1) Based on extrapolation. Estimated global s

f 35 o diversity of true freshwater crabs: 2,155 species r 30 e b

Yeo & Ng (1999) used the species number per unit m 25 u

À4 2 n 20 area of Thailand (1.8 · 10 species/km )asa e v i

t 15 a reference for estimating the fauna for the whole of l

u 10 m

Indochina. These authors applied this ratio to Indo- u 5 C china [=Thailand, Laos, Cambodia, Vietnam and 0 0 0 0 0 0 0 0 0 5 0 4 2 0 5 0 5 6 7 8 9 9 0 0 8 8 9 9 9 9 9 9 9 0 0 Myanmar] (1,939,320 km ), and obtained a working 1 1 1 1 1 1 1 1 1 2 2 ------3 1 1 1 1 1 1 1 1 6 1 8 0 5 0 5 6 7 8 9 9 0 7 8 8 9 9 9 9 9 9 9 0 estimate of 349 species for this region. There are 1 1 1 1 1 1 1 1 1 1 2 currently 212 species known from Indochina (Yeo & Period Ng, unpub.) which gives an approximate ratio of Fig. 2 Cumulative number of South American species of: (a) actual to estimated species of 1:1.65. The 13 species Pseudothelphusidae described since 1840; and (b) Trichodac- of freshwater crabs known from Madagascar give a tylidae described since 1783 similar estimate (Cumberlidge & Sternberg, 2002). Although simplistic, no similar objective estimates margins of South America produced many vicariance have been attempted thus far. Applying a ratio of events (Lundberg et al., 1998) that could account for actual to estimated species of 1:1.65 to the known the high diversiﬁcation of the pseudothelphusids true freshwater crab global diversity from the previ- along the Andes. Pseudothelphusids are usually ous section (1,306 species), gives an estimated global distributed in mountainous regions with restricted diversity of 2,155 species. Given that Indochina lies distributional ranges and there still are several in one of the most species-rich areas of the global unexplored areas in the Andes, Guyana and the range of freshwater crabs, this ﬁgure may tend to be Central Brazilian Massifs from where new taxa are an overestimate. Considering the large numbers of still being found. Species of trichodactylids usually undescribed species known and/or likely to be have extensive ranges along the relatively uniform, discovered in the near future, freshwater crab taxon- tectonically stable lowlands of the continent’s huge omy must be regarded as still being in its hydrographic basins, have not speciated as much as ‘‘discovery’’ phase. The cumulative curves of new the pseudothelphusids, and the number of new species described over time for the two South species of trichodactylids still awaiting discovery is American crab families suggests that the diversity expected to be low. of the Pseudothelphusidae is still far from being well- (2) Based on numbers of as yet undescribed known because the curve (Fig. 2a) is still ascending. species known. Estimated global diversity of true On the other hand, the curve for the trichodactylids freshwater crabs: 1,430 species. (Fig. 2b) seems to have already reached an asymp- This estimate is based simply on the total number tote, suggesting at least for this group, the discovery of described and undescribed species of true fresh- phase is ending. The several phases of tectonic uplift water crabs known to the authors. The breakdown of that affected most of the western and northern these estimates by family is as follows: Potamidae 123 280 Hydrobiologia (2008) 595:275–286

(570 species); Potamonautidae (135 species); Decke- crabs are endemic to their respective zoogeographical niidae (3 species); Platythelphusidae (12 species); regions (sensu Cox, 2001; see below). Parathelphusidae (310 species); Gecarcinucidae (60 The distribution of freshwater crab diversity across species); Pseudothelphusidae (289 species) and the main zoogeographical regions (sensu Cox, 2001) Trichodactylidae (51 species). The disparity between adopted in this volume is illustrated in Table 1 the overall estimates obtained using this method (species), Table 2 (genera), and Fig. 3 (total and true versus the extrapolation method is probably accentu- freshwater crabs). It should be noted, however, that ated by the fact that some of our family level the phylogeographical patterns of some taxa are not estimates here are conservative. Reality is probably always reﬂected by this categorisation. One such somewhere in between, which means that there are at anomaly is with the family Potamidae, in which the least 128–846 more species yet to be described/ two subfamilies have relatively distinct distributions: discovered. A more accurate system of estimating Potaminae is clearly a Palaearctic group with the species numbers is clearly needed. main diversity in southern Europe/North Africa/Near East/Middle East, while Potamiscinae is an Oriental group with the main diversity in East and Southeast Distribution and zoogeography Asia. These two groups are only linked by the potamids of the northwestern Oriental Region, where The vast majority of true freshwater crab species are their distributions overlap around parts of Myanmar point endemics owing to their generally limited and northeastern India (Yeo & Ng, 2003). Following dispersal abilities, relatively low fecundity, and strictly the zoogeographical regions of Cox (2001), stenotopic habits. Most genera of true freshwater however, a signiﬁcant proportion of East Asian

Fig. 3 Map of zoogeographical regions sensu Cox (2001) parentheses. (PA—Palaearctic; NA—Nearctic; AT—Afrotropical; showing total freshwater crab distribution (Species number/ NT—Neotropical; OL—Oriental; AU—Australasian; PAC— Genus number). True freshwater crab distribution is shown in Pacific Oceanic Islands; ANT—Antartica) 123 Hydrobiologia (2008) 595:275–286 281 potamiscines will fall into the Palaearctic region taxa with this character are found today in the (together with potamines) instead. majority of Gondwanan fragments (South America, Furthermore, a small group (two genera with three Africa, Madagascar, the Seychelles, India, Southeast species) of potamids on the island of Socotra off the Asia, and Australasia). Crabs are postulated to have horn of Africa that is clearly affiliated with the had a Gondwanan origin with present day distribution Paleartctic potamines falls misleadingly under the patterns resulting from the breakup of the supercon- Afrotropical region instead. Similarly, the definition tinent (Rodrı´guez, 1986; Ng & Rodrı´guez, 1995;Ng in this volume of the Neotropical region as ‘‘excluding et al., 1995; Yeo & Ng, 1999). There is, however, no highlands of Mexico’’ and the Nearctic as ‘‘including paleontological support for this view and there is highlands of Mexico’’, ends up assigning pseudothel- incongruence with regard to what is known about phusids found in the Mexican highlands to the Brachyuran evolution. Daniels et al. (2006), how- Nearctic region despite their Neotropical affinities. ever, argue that the two-segmented bilobed In addition, not all taxa are restricted to a single mandibular palp may be a convergent character, zoogeographical region (e.g. Aparapotamon grahami and the pseudothelphusoid and gecarcinucoids may and Geothelphusa spp. [Potamidae] occur in both not be that closely related. Ba˘na˘rescu (1990) pro- Palaearctic and Oriental regions; and Parathelphusa posed long distance transoceanic dispersal as an and Sundathelphusa [Parathelphusidae] occur in both alternative mechanism to explain the largely insular Oriental and Australasian regions). The families distribution of the Parathelphusidae in Sundaic containing species and/or genera that have distribu- Southeast Asia. However, this has been challenged tions which overlap adjacent zoogeographical regions by Ng & Rodrı´guez (1995), who argued that are: Potamidae, Parathelphusidae, Pseudothelphusi- Ba˘na˘rescu’s ideas made dubious assumptions about dae, Gecarcinidae, Hymenosomatidae, Sesarmidae, the ecology and origins of the Parathelphusidae (and Goneplacidae and Varunidae. Because of this, as about the phylogeny of all freshwater crabs). The mentioned earlier, the ‘‘World’’ totals listed in the last dominance of gecarcinucoid crabs in the Indian column of Tables 1 and 2 for these families are less peninsula (and the absence of potamids) could also than the sum of the number of taxa from each be explained as the result of their long isolation on a zoogeographical region on the map (Fig. 3) or in the Gondwanan continental fragment before it collided corresponding row of each table (see Tables 1 and 2 with continental Asia (where potamids are found in footnotes). large numbers). In contrast to the above hypotheses, the phylogenetic school (Sternberg et al., 1999, following Major historic processes leading to global Colosi’s (1921) ideas) suggested that the pseud- biodiversity patterns othelphusoid, gecarcinucoid, and potamoid freshwater crabs form a monophyletic group that Sternberg et al. (1999) summarised the hypotheses may have had a more recent, post-Gondwanan for the origin and diversification of the true freshwa- origin. Here the present global distribution pattern ter crabs into the polyphyletic, archaic and is thought to be the result of colonisation of the phylogenetic schools. The polyphyletic school (e.g. tropical continental margins from a common ances- Bott, 1955; Pretzmann, 1973) considered that the tral marine group consisting of a monophyletic freshwater crab families originated from a number of thoracotreme clade widely distributed along littoral different marine ancestors; in this case, morpholog- areas of the southern Tethys Sea during the Creta- ical similarities would be the result of convergence, ceous that eventually gave rise to the modern not common ancestry. families after independent diversification into the In the archaic population school, vicariance has freshwater environments. This post-Gondwanan been suggested as the key mechanism and the (Cretaceous) transoceanic dispersal hypothesis was breakup of Gondwanaland a key historic process. most recently supported by molecular evidence The pseudothelphusoid and gecarcinucoid freshwater presented by Daniels et al. (2006) based on work crabs share a two-segmented bilobed mandibular palp carried out with emphasis on Afrotropical freshwater (a presumptive synapomorph) and freshwater crab crabs. Another hypothesis recently proposed by 123 282 Hydrobiologia (2008) 595:275–286

Klaus et al. (2006) suggested that gecarcinucoid Potamocarcinini), northern and eastern South Amer- crabs originated in Africa and reached South Asia ica (Kingsleyini) and the southern Andes via transoceanic dispersal and a series of theorised (Hypolobocerini). ‘‘stepping-stone’’ islands. The available evidence The South American trichodactylids are phyloge- might now suggest a mixture of vicariance and netically separate from all other freshwater crab dispersal, although consensus has still to be reached families which points to an independent invasion of in this complex issue. Clearly, there are many ideas this habitat by the group’s supposedly marine portu- and hypotheses being proposed, a sure sign that noid ancestors (Rodrı´guez, 1992; Sternberg et al., there is increasing interest in using freshwater crabs 1999; Martin & Davis, 2001). The morphological for biogeographic studies. cladistic analysis of Sternberg et al. (1999) identified The current Eurasian distribution of the Potamidae grapsids as probable sister taxa to the non-tricho- shows that one subfamily (Potaminae) occurs in dactylid freshwater crabs, which contradicted the western Eurasia (in North Africa, southern Europe, assertions of earlier authors (Bott, 1955) who Socotra, the Middle East and the Himalayas), and one suggested ancestry from marine crab groups such as subfamily (the Potamiscinae) is in Southeast Asia, the Xanthoidea or the Portunoidea. There is, how- China and Japan. There is reason to believe that this ever, still some uncertainty about freshwater crab distributional pattern may be the result of dispersal origins and relationships. from a continental Asian origin (Yeo & Ng, 2003). A In addition to vicariance and dispersal, distribu- trend is apparent in the relative distributions of these tional limits of true freshwater crabs are also two subfamilies that suggests potamids may have influenced by a host of other factors that interact spread westwards into Eurasia (as potamines) and with these two key processes. These include abiotic southwards into insular Southeast Asia (as potamis- factors such as climate, hydrology, topography and cines) from a continental Asian origin. Additional altitude as well as biotic factors such as habitat circumstantial evidence for this trend is seen in the vegetation and inter-specific competition (see Rodrı´- distinct decline in potamid diversity westward from guez, 1986; Ng, 1988; Barbaresi & Gherardi, 1997; Southeast Asia, whereby southern Europe has only Cumberlidge, 1999; Dai, 1999; Rodrı´guez & Sua´rez, one genus (Potamon) and East Asia has some 40 2004; Magalha˜es et al., 2005; Marijnissen et al., genera. The distributional trend shown by potamines 2005). and potamiscines corresponds to a similar trend shown by freshwater crab superfamilies discussed by Yeo & Ng (1999). Phylogeny Rodrı´guez (1982, 1986) explained the current distribution of Neotropical pseudothelphusids by The recent surge in alpha taxonomic descriptions of vicariance events and secondary dispersion. In his freshwater crabs has been accompanied by an hypothesis, based on Rosen’s (1976) model for increase in interest in their phylogenetic relation- Caribbean biogeography, an ancestral group that ships and higher taxonomy. Most studies in the late occupied the Proto-Antillean archipelago, character- 20th century have accepted the traditional morphol- ised by a plesiomorphic character of the third ogy-based classification system proposed by Bott maxilliped (presence of long exognath), gave rise to (1970) comprising three superfamilies and eleven two different groups after the Caribbean Plate drifted families. This has been challenged over the last northeastward between Central and South America decades by some workers who questioned the during the late Mesozoic and Cenozoic: the Epilobo- superfamily system and synonymised three families, cerinae in the Antilles and the Strengerianini in namely Sundathelphusidae, now a junior synonym northern Colombia. Based on sympatries and geo- of Parathelphusidae (Ng, 1988; Chia & Ng, 1998); graphic morphoclines in somatic and gonopodal and Isolapotamidae and Sinopotamidae, both now characters, Rodrı´guez (1986) distinguished three junior synonyms of Potamidae (Ng, 1988; Dai, distinct chorological series that would have radiated 1999; Yeo & Ng, 2003). Brandis (2002) had from a dispersal centre in northern Colombia towards recently argued for the revalidation of the families Central America and Mexico (Pseudothelphusini and Isolapotamidae and Sinopotamidae for two 123 Hydrobiologia (2008) 595:275–286 283 apparently discreet monophyletic potamid taxa; of the Tertiary for the African Potamonautidae. Later, however, this was challenged by Yeo & Ng (2003) in agreement with Rodrı´guez (1986) that New World who suggested that Brandis’ (2002) groupings might pseudothelphusoids and Old World gecarcinucoids instead be infra-familial clades within the Potamidae share a synapomorphy (a bilobed mandibular palp), (subfamily Potamiscinae). Ng et al. (1995) suggested that the freshwater crabs Morphological cladistic studies (e.g. Sternberg possessing this synapomorph were at least 120 mil- et al., 1999; Cumberlidge, 1999; Sternberg & lion years old by inference, corresponding to the Cumberlidge, 1999, 2001) argue for recognising timing of the split between South America and the remaining eight families in two main lineages. Africa. More recently, Daniels et al. (2006) estimated These authors argued that the true freshwater crabs that Afrotropical crabs radiated some 75.03– are paraphyletic and consist of two distinct lineages: 78.6 million years ago. The fossil evidence, however, (1) the monophyletic Trichodactylidae in the pre- does not support any of the above proposed age dominantly marine superfamily Portunoidea and (2) estimates, with the oldest known fossil from the a monophyletic group consisting of all remaining Upper Tertiary in northern India and Europe being freshwater crab families assigned to three superfam- not much older than 23 mya (Bott, 1955; Glaessner, ilies, viz., Potamoidea (Potamidae, Potamonautidae, 1969). Ng et al. (1995), however, warned against Deckeniidae, Platythelphusidae), Gecarcinucoidea making firm conclusions based on this dearth of (Parathelphusidae, Gecarcinucidae) and Pseudothel- fossils, commenting that, ‘‘the rarity and difficulty of phusoidea (Pseudothelphusidae). Various authors forming (and finding) freshwater fossils is well have expressed doubts about the existing family known’’. classification and it is clear that there is still much to One of the key processes driving freshwater crab be done before a reasonable consensus can be diversification is likely to be allopatric speciation reached. Most recently, Daniels et al. (2006) have resulting from geographic isolation. This is helped suggested that some of these families may be by the relatively low fecundity and poor dispersal artificial, while Brandis (2002), and Klaus et al. abilities of freshwater crabs; and is often facilitated (2006) and Cumberlidge et al. (2007) have each by the habitat heterogeneity and numerous ecolog- offered different systems of higher classification. ical niches and microhabitats afforded by the We have erred on the side of ‘‘conservativeness’’ in complicated topography and hydrology of their the system adopted here. The differences between workers will only encourage more morphological and molecular work to help resolve the conflicting views to the classification of these animals. Cur- rently, there are few other molecular phylogenies of freshwater crabs and those available have a limited geographical scope (e.g. Japan: Segawa, 2000; Taiwan: Shih et al., 2004, 2007; South Africa: Daniels et al., 2002; India and Sri Lanka: Bossuyt et al., 2004; East Africa: Marijnissen et al., 2006; Malay Peninsula: Yeo et al., 2007). The status of the phylogenetic relationships of the freshwater crabs is, therefore, still controversial in the face of incongru- ent morphological and molecular studies and is the subject of ongoing work by several research groups including the present authors. For convenience, we follow the higher taxonomy of the freshwater crabs proposed by Martin & Davis (2001). Bott (1955) estimated that the age of freshwater Fig. 4 Freshwater crabs (Somanniathelphusa dangi: Parathel- crabs was about 65 million years, with an origin phusidae) being sold as food in a rural market in northern between the end of the Cretaceous and the beginning Vietnam 123 284 Hydrobiologia (2008) 595:275–286 environments. Nevertheless, the significance of the freshwater crab fauna, however, is low as demand sympatric speciation cannot be discounted, espe- is low and collection irregular. cially for lacustrine species (e.g. Platythelphusa in the African Rift Valley Lakes (Cumberlidge et al., 1999; Marijnissen et al., 2006); and Parathelphusa Threats and conservation issues and allies in the Sulawesi lakes (Chia & Ng, 2006)). All these factors have led to a high degree of Based on a recent assessment of the conservation status endemism in freshwater crabs. of Malaysian freshwater crabs, a few patterns emerged (Ng & Yeo, 2007). The restricted distributions of most of the freshwater crab species pose serious problems Human-related issues for conservation. Fortunately, for the time being, the species with the most restricted distributions are often Economic and medical uses those that inhabit offshore islands or mountains, areas that are generally less immediately impacted by man. Freshwater crabs are an important protein source and The loss of natural forest as a result of land develop- are consumed in many parts of the world. Ng (1988) ment and agriculture has generally affected lowlands noted that in Thailand, large potamids and parathel- more severely. However, many lowland species (e.g. phusids are occasionally eaten by locals. Yeo & Ng Parathelphusa maculata) may have survived because (1998) commented that potamids are important in the they have relatively wider distributions. Specialist diet of rural and hill tribes of northern Vietnam species (e.g. obligate cavernicoles like Cerberusa (Fig. 4). Freshwater crabs are also consumed for caeca), and highland taxa (e.g. Johora grallator)are purported medicinal and tonic properties, including at higher risk because they have a restricted range and treatment of stomach ailments and physical injuries are less tolerant of habitat changes. A similar study was (Dai, 1999). In South America, indigenous groups use made of the Sri Lankan fauna by Bahir et al. (2005), freshwater crabs, particularly large pseudothelphus- and of the Tanzanian and Southern African freshwater ids, for food (Finkers 1986). crabs by Reed & Cumberlidge (2006) and Cumberlidge Medically, freshwater crabs are important because & Daniels (2007). they are intermediate hosts to the parasitic lung fluke, The conservation of freshwater crabs will depend Paragonimus (Platyhelminthes) which causes par- primarily on preserving large enough natural forest agonimiasis. This dangerous disease affects humans areas to maintain the good water quality of the when they consume infected crabs (Ng, 1988; Dai, original streams. Thus, the need to establish more 1999; Cumberlidge, 1999). Rodrı´guez & Magalha˜es nature reserves and national parks, together with (2005) listed the pseudothelphusid species reported as careful planning and development is imperative. hosts for Paragonimus and discussed its occurrence in the neotropics. Although proper cooking would kill Acknowledgements This study has benefited from the help the parasite, many of the more rural communities and advice from many colleagues. We thank Tohru Naruse and Paul Clark for their many helpful comments and suggestions prefer to consume freshwater crabs half-raw (Ng, which have helped improve the manuscript. Support from the 1988; Dai, 1999). Belgium Biodiversity Platform, the Belgian Science Policy, the Freshwater crabs are sometimes sold in the Royal Belgium Institute of Natural Sciences, and the aquarium trade. These are usually the more colourful Department of Biological Sciences, National University of Singapore, is gratefully acknowledged. Indochinese potamids e.g. Demanietta khirikhan, Pudaengon arnamicai, Terrapotamon abbotti, although less gaudy parathelphusids like Heterothel- phusa fatum are also sold. The trichodactylid crab, References Dilocarcinus pagei, is captured for bait in game fishing of large catfishes in the Pantanal Matogros- Bahir, M. M., P. K. L. Ng, K. Crandall & R. Pethiyagoda, 2005. A conservation assessment of the freshwater crabs sense, a swampy area in the Paraguay River basin of Sri Lanka. Raffles Bulletin of Zoology Supplement 12: (Magalha˜es, 2000). The impact of these activities on 121–126.

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